Healthy lifestyle and the risk of lymphoma in the European Prospective Investigation into Cancer and Nutrition study
Sabine Naudin
Nutritional Methodology and Biostatistics Group, International Agency for Research on Cancer, World Health Organization, Lyon, France
Search for more papers by this authorMarta Solans Margalef
Centro de Investigación Biomédica en Red: Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
Research Group on Statistics, Econometrics and Health (GRECS), University of Girona, Girona, Spain
Search for more papers by this authorFatemeh Saberi Hosnijeh
Institute for Risk Assessment Sciences, Division of Environmental Epidemiology, Utrecht University, Utrecht, The Netherlands
Search for more papers by this authorAlexandra Nieters
Research Group Epidemiology, Institute for Immunodeficiency, Medical Center-University of Freiburg, Freiburg, Germany
Search for more papers by this authorCecilie Kyrø
Danish Cancer Society Research Center, Copenhagen, Denmark
Search for more papers by this authorAnne Tjønneland
Danish Cancer Society Research Center, Copenhagen, Denmark
Department of Public Health, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorChristina C. Dahm
Section for Epidemiology, Department of Public Health, Aarhus University, Aarhus, Denmark
Search for more papers by this authorKim Overvad
Section for Epidemiology, Department of Public Health, Aarhus University, Aarhus, Denmark
Department of Cardiology, Aalborg University Hospital, Aalborg, Denmark
Search for more papers by this authorYahya Mahamat-Saleh
CESP, Faculté de Médecine, Université Paris-Sud, UVSQ, INSERM, Université Paris-Saclay, Villejuif, France
Gustave Roussy, Villejuif, France
Search for more papers by this authorCaroline Besson
CESP, Faculté de Médecine, Université Paris-Sud, UVSQ, INSERM, Université Paris-Saclay, Villejuif, France
Department of Hematology and Oncology, Hospital of Versailles, Le Chesnay, France
Search for more papers by this authorMarie-Christine Boutron-Ruault
CESP, Faculté de Médecine, Université Paris-Sud, UVSQ, INSERM, Université Paris-Saclay, Villejuif, France
Gustave Roussy, Villejuif, France
Search for more papers by this authorTilman Kühn
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
Search for more papers by this authorFederico Canzian
Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany
Search for more papers by this authorMatthias B. Schulze
Department of Molecular Epidemiology, German Institute of Human Nutrition, Nuthetal, Germany
Institute of Nutrition Science, University of Potsdam, Nuthetal, Germany
Search for more papers by this authorAnna Karakatsani
Hellenic Health Foundation, Athens, Greece
Pulmonary Medicine Department, School of Medicine, National and Kapodistrian University of Athens, “ATTIKON” University Hospital, Haidari, Greece
Search for more papers by this authorAntonia Trichopoulou
Hellenic Health Foundation, Athens, Greece
Search for more papers by this authorSabina Sieri
Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy
Search for more papers by this authorGiovana Masala
Cancer Risk Factors and Life-Style Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network – ISPRO, Florence, Italy
Search for more papers by this authorSalvatore Panico
Department of Clinical and Experimental Medicine, University Federico II, Naples, Italy
Search for more papers by this authorRosario Tumino
Cancer Registry and Histopathology Department, Azienda Sanitaria Provinciale (ASP) Ragusa, Ragusa, Italy
Search for more papers by this authorFulvio Ricceri
Department of Clinical and Biological Sciences, University of Turin, Turin, Italy
Unit of Epidemiology, Regional Health Service ASL TO3, Grugliasco (TO), Italy
Search for more papers by this authorSairah L.F. Chen
Institutt for Samfunnsmedisin, Det Helsevitenskapelige fakultet, UiT, Norges Arktiske Universitet, Tromso, Norway
Search for more papers by this authorLeila L. Barroso
Unit of Nutrition and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO-IDIBELL), Barcelona, Spain
Search for more papers by this authorJosé M. Huerta
Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain
Spanish Consortium for Research and Public Health (CIBERESP), Madrid, Spain
Search for more papers by this authorMaria-Jose Sánchez
Spanish Consortium for Research and Public Health (CIBERESP), Madrid, Spain
Andalusian School of Public Health (EASP), Granada, Spain
Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
Universidad de Granada (UGR), Granada, Spain
Search for more papers by this authorEva Ardanaz
Spanish Consortium for Research and Public Health (CIBERESP), Madrid, Spain
Navarra Public Health Institute, Pamplona, Spain
IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
Search for more papers by this authorPilar Amiano Exezarreta
Spanish Consortium for Research and Public Health (CIBERESP), Madrid, Spain
Public Health Division of Gipuzkoa, Biodonostia Health Research Institute, Ministry of Health of the Basque Government, San Sebastian, Spain
Search for more papers by this authorFlorentin Spaeth
Department of Radiation Sciences and Oncology, Umeå University, Umeå, Sweden
Search for more papers by this authorMats Jerkeman
Division of Oncology, Lund University, Malmö, Sweden
Search for more papers by this authorKarin Jirstom
Department of Clinical Sciences Lund, Oncology and Therapeutic Pathology, Lund University, Lund, Sweden
Search for more papers by this authorJulie A. Schmidt
Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorDagfinn Aune
Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom
Department of Nutrition, Bjørknes University College, Oslo, Norway
Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo University Hospital, Oslo, Norway
Search for more papers by this authorElisabete Weiderpass
Office of the Director, International Agency for Research on Cancer, World Health Organization, Lyon, France
Search for more papers by this authorElio Riboli
Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom
Search for more papers by this authorRoel Vermeulen
Institute for Risk Assessment Sciences, Division of Environmental Epidemiology, Utrecht University, Utrecht, The Netherlands
Search for more papers by this authorDelphine Casabonne
Centro de Investigación Biomédica en Red: Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
Unit of Molecular and Genetic Epidemiology in Infections and Cancer, Catalan Institute of Oncology (ICO-IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain
Search for more papers by this authorMarc Gunter
Nutritional Epidemiology Group, International Agency for Research on Cancer, World Health Organization, Lyon, France
Search for more papers by this authorPaul Brennan
Genetic Epidemiology Group, International Agency for Research on Cancer, World Health Organization, Lyon, France
Search for more papers by this authorCorresponding Author
Pietro Ferrari
Nutritional Methodology and Biostatistics Group, International Agency for Research on Cancer, World Health Organization, Lyon, France
Correspondence to: Pietro Ferrari, E-mail: [email protected]Search for more papers by this authorSabine Naudin
Nutritional Methodology and Biostatistics Group, International Agency for Research on Cancer, World Health Organization, Lyon, France
Search for more papers by this authorMarta Solans Margalef
Centro de Investigación Biomédica en Red: Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
Research Group on Statistics, Econometrics and Health (GRECS), University of Girona, Girona, Spain
Search for more papers by this authorFatemeh Saberi Hosnijeh
Institute for Risk Assessment Sciences, Division of Environmental Epidemiology, Utrecht University, Utrecht, The Netherlands
Search for more papers by this authorAlexandra Nieters
Research Group Epidemiology, Institute for Immunodeficiency, Medical Center-University of Freiburg, Freiburg, Germany
Search for more papers by this authorCecilie Kyrø
Danish Cancer Society Research Center, Copenhagen, Denmark
Search for more papers by this authorAnne Tjønneland
Danish Cancer Society Research Center, Copenhagen, Denmark
Department of Public Health, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorChristina C. Dahm
Section for Epidemiology, Department of Public Health, Aarhus University, Aarhus, Denmark
Search for more papers by this authorKim Overvad
Section for Epidemiology, Department of Public Health, Aarhus University, Aarhus, Denmark
Department of Cardiology, Aalborg University Hospital, Aalborg, Denmark
Search for more papers by this authorYahya Mahamat-Saleh
CESP, Faculté de Médecine, Université Paris-Sud, UVSQ, INSERM, Université Paris-Saclay, Villejuif, France
Gustave Roussy, Villejuif, France
Search for more papers by this authorCaroline Besson
CESP, Faculté de Médecine, Université Paris-Sud, UVSQ, INSERM, Université Paris-Saclay, Villejuif, France
Department of Hematology and Oncology, Hospital of Versailles, Le Chesnay, France
Search for more papers by this authorMarie-Christine Boutron-Ruault
CESP, Faculté de Médecine, Université Paris-Sud, UVSQ, INSERM, Université Paris-Saclay, Villejuif, France
Gustave Roussy, Villejuif, France
Search for more papers by this authorTilman Kühn
Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany
Search for more papers by this authorFederico Canzian
Genomic Epidemiology Group, German Cancer Research Center (DKFZ), Heidelberg, Germany
Search for more papers by this authorMatthias B. Schulze
Department of Molecular Epidemiology, German Institute of Human Nutrition, Nuthetal, Germany
Institute of Nutrition Science, University of Potsdam, Nuthetal, Germany
Search for more papers by this authorAnna Karakatsani
Hellenic Health Foundation, Athens, Greece
Pulmonary Medicine Department, School of Medicine, National and Kapodistrian University of Athens, “ATTIKON” University Hospital, Haidari, Greece
Search for more papers by this authorAntonia Trichopoulou
Hellenic Health Foundation, Athens, Greece
Search for more papers by this authorSabina Sieri
Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy
Search for more papers by this authorGiovana Masala
Cancer Risk Factors and Life-Style Epidemiology Unit, Institute for Cancer Research, Prevention and Clinical Network – ISPRO, Florence, Italy
Search for more papers by this authorSalvatore Panico
Department of Clinical and Experimental Medicine, University Federico II, Naples, Italy
Search for more papers by this authorRosario Tumino
Cancer Registry and Histopathology Department, Azienda Sanitaria Provinciale (ASP) Ragusa, Ragusa, Italy
Search for more papers by this authorFulvio Ricceri
Department of Clinical and Biological Sciences, University of Turin, Turin, Italy
Unit of Epidemiology, Regional Health Service ASL TO3, Grugliasco (TO), Italy
Search for more papers by this authorSairah L.F. Chen
Institutt for Samfunnsmedisin, Det Helsevitenskapelige fakultet, UiT, Norges Arktiske Universitet, Tromso, Norway
Search for more papers by this authorLeila L. Barroso
Unit of Nutrition and Cancer, Cancer Epidemiology Research Program, Catalan Institute of Oncology (ICO-IDIBELL), Barcelona, Spain
Search for more papers by this authorJosé M. Huerta
Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain
Spanish Consortium for Research and Public Health (CIBERESP), Madrid, Spain
Search for more papers by this authorMaria-Jose Sánchez
Spanish Consortium for Research and Public Health (CIBERESP), Madrid, Spain
Andalusian School of Public Health (EASP), Granada, Spain
Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Granada, Spain
Universidad de Granada (UGR), Granada, Spain
Search for more papers by this authorEva Ardanaz
Spanish Consortium for Research and Public Health (CIBERESP), Madrid, Spain
Navarra Public Health Institute, Pamplona, Spain
IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
Search for more papers by this authorPilar Amiano Exezarreta
Spanish Consortium for Research and Public Health (CIBERESP), Madrid, Spain
Public Health Division of Gipuzkoa, Biodonostia Health Research Institute, Ministry of Health of the Basque Government, San Sebastian, Spain
Search for more papers by this authorFlorentin Spaeth
Department of Radiation Sciences and Oncology, Umeå University, Umeå, Sweden
Search for more papers by this authorMats Jerkeman
Division of Oncology, Lund University, Malmö, Sweden
Search for more papers by this authorKarin Jirstom
Department of Clinical Sciences Lund, Oncology and Therapeutic Pathology, Lund University, Lund, Sweden
Search for more papers by this authorJulie A. Schmidt
Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorDagfinn Aune
Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom
Department of Nutrition, Bjørknes University College, Oslo, Norway
Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo University Hospital, Oslo, Norway
Search for more papers by this authorElisabete Weiderpass
Office of the Director, International Agency for Research on Cancer, World Health Organization, Lyon, France
Search for more papers by this authorElio Riboli
Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom
Search for more papers by this authorRoel Vermeulen
Institute for Risk Assessment Sciences, Division of Environmental Epidemiology, Utrecht University, Utrecht, The Netherlands
Search for more papers by this authorDelphine Casabonne
Centro de Investigación Biomédica en Red: Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
Unit of Molecular and Genetic Epidemiology in Infections and Cancer, Catalan Institute of Oncology (ICO-IDIBELL), L'Hospitalet de Llobregat, Barcelona, Spain
Search for more papers by this authorMarc Gunter
Nutritional Epidemiology Group, International Agency for Research on Cancer, World Health Organization, Lyon, France
Search for more papers by this authorPaul Brennan
Genetic Epidemiology Group, International Agency for Research on Cancer, World Health Organization, Lyon, France
Search for more papers by this authorCorresponding Author
Pietro Ferrari
Nutritional Methodology and Biostatistics Group, International Agency for Research on Cancer, World Health Organization, Lyon, France
Correspondence to: Pietro Ferrari, E-mail: [email protected]Search for more papers by this authorAbstract
Limited evidence exists on the role of modifiable lifestyle factors on the risk of lymphoma. In this work, the associations between adherence to healthy lifestyles and risks of Hodgkin lymphoma (HL) and non-Hodgkin lymphoma (NHL) were evaluated in a large-scale European prospective cohort. Within the European Prospective Investigation into Cancer and Nutrition (EPIC), 2,999 incident lymphoma cases (132 HL and 2,746 NHL) were diagnosed among 453,808 participants after 15 years (median) of follow-up. The healthy lifestyle index (HLI) score combined information on smoking, alcohol intake, diet, physical activity and BMI, with large values of HLI expressing adherence to healthy behavior. Cox proportional hazards models were used to estimate lymphoma hazard ratios (HR) and 95% confidence interval (CI). Sensitivity analyses were conducted by excluding, in turn, each lifestyle factor from the HLI score. The HLI was inversely associated with HL, with HR for a 1-standard deviation (SD) increment in the score equal to 0.78 (95% CI: 0.66, 0.94). Sensitivity analyses showed that the association was mainly driven by smoking and marginally by diet. NHL risk was not associated with the HLI, with HRs for a 1-SD increment equal to 0.99 (0.95, 1.03), with no evidence for heterogeneity in the association across NHL subtypes. In the EPIC study, adherence to healthy lifestyles was not associated with overall lymphoma or NHL risk, while an inverse association was observed for HL, although this was largely attributable to smoking. These findings suggest a limited role of lifestyle factors in the etiology of lymphoma subtypes.
Abstract
What's new?
Do lifestyle factors affect lymphoma risk? Previous studies have been inconclusive, and most lacked statistical power to allow accurate conclusions. In this large, prospective European study, the authors examined the relationship between a score combining lifestyle exposures, such as smoking, BMI, and alchohol, and the risk of lymphoma. They observed that healthy behaviors were inversely related to the risk of Hodgkin lymphoma, although smoking was the main driver of the association. These findings indicated a limited role for lifestyle factors in the etiology of lymphomas.
Conflict of interest
None to declare.
Supporting Information
| Filename | Description |
|---|---|
| ijc32977-sup-0001-Supinfo.pdfPDF document, 152.8 KB | Appendix S1. Supporting Information. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1Turner JJ, Morton LM, Linet MS, et al. InterLymph hierarchical classification of lymphoid neoplasms for epidemiologic research based on the WHO classification (2008): update and future directions. Blood 2010; 116: e90–8.
- 2Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68: 394–424.
- 3Evens AM, Antillón M, Aschebrook-Kilfoy B, et al. Racial disparities in Hodgkin's lymphoma: a comprehensive population-based analysis. Ann Oncol 2012; 23: 2128–37.
- 4 World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Expert Report 2018. Diet, nutrition, physical activity and pancreatic cancer. Washington, DC: WCRF/AICR. Available from: www.dietandcancerreport.org, 2018.
- 5 IARC. Absence of Excess Body Fatness/IARC Working Group on the Evaluation of Cancer-Preventive Interventions. IARC Handbooks of Cancer Prevention. Lyon, France: IARC, 2018. 658 Available from: http://publications.iarc.fr/570.
- 6Bagnardi V, Rota M, Botteri E, et al. Alcohol consumption and site-specific cancer risk: a comprehensive dose–response meta-analysis. Br J Cancer 2015; 112: 580–93.
- 7McKenzie F, Biessy C, Ferrari P, et al. Healthy lifestyle and risk of cancer in the European prospective investigation into cancer and nutrition cohort study. Medicine (Baltimore) 2016; 95:e2850.
- 8Riboli E, Hunt KJ, Slimani N, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr 2002; 5: 1113–24.
- 9Ferrari P, Day NE, Boshuizen HC, et al. The evaluation of the diet/disease relation in the EPIC study: considerations for the calibration and the disease models. Int J Epidemiol 2008; 37: 368–78.
- 10Schoenfeld D. Partial residuals for the proportional hazards regression model. Biometrika 1982; 69: 239–41.
- 11Heinzl H, Kaider A. Gaining more flexibility in Cox proportional hazards regression models with cubic spline functions. Comput Methods Programs Biomed 1997; 54: 201–8.
- 12Lunn M, McNeil D. Applying cox regression to competing risks. Biometrics 1995; 51: 524–32.
- 13 StataCorp. Stata statistical software: release 14. College Station, TX: StataCorp LP, 2015.
- 14Kabat GC, Matthews CE, Kamensky V, et al. Adherence to cancer prevention guidelines and cancer incidence, cancer mortality, and total mortality: a prospective cohort study. Am J Clin Nutr 2015; 101: 558–69.
- 15Sergentanis T, Kanavidis P, Michelakos T, et al. Cigarette smoking and risk of lymphoma in adults. Eur J Cancer Prev 2013; 22: 131–50.
- 16Mehta H, Nazzal K, Sadikot RT. Cigarette smoking and innate immunity. Inflamm Res 2008; 57: 497–503.
- 17Epstein MM, Chang ET, Zhang Y, et al. Dietary pattern and risk of hodgkin lymphoma in a population-based case-control study. Am J Epidemiol 2015; 182: 405–16.
- 18Solans M, Benavente Y, Saez M, et al. Inflammatory potential of diet and risk of lymphoma in the European Prospective Investigation into Cancer and Nutrition. Eur J Nutr 2019; 59: 813–23.
- 19Solans M, Benavente Y, Saez M, et al. Adherence to the mediterranean diet and lymphoma risk in the european prospective investigation into cancer and nutrition. Int J Cancer 2019; 145: 122–31.
- 20Biggar RJ, Johansen JS, Smedby KE, et al. Serum YKL-40 and interleukin 6 levels in Hodgkin lymphoma. Clin Cancer Res 2008; 14: 6974–8.
- 21Abar L, Sobiecki JG, Cariolou M, et al. Body size and obesity during adulthood, and risk of lympho-haematopoietic cancers: an update of the WCRF-AICR systematic review of published prospective studies. Ann Oncol 2019; 30: 528–41.
- 22Bryant AJ, Newman JH. Alcohol intolerance associated with Hodgkin lymphoma. CMAJ 2013; 185:E353.
- 23Swerdlow S, Campo E, Harris N, et al. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Lyon, France: IARC, 2017 Available from: http://publications.iarc.fr/Book-And-Report-Series/Who-Iarc-Classification-Of-Tumours/Who-Classification-Of-Tumours-Of-Haematopoietic-And-Lymphoid-Tissues-2017. Accessed July 9, 2018.
- 24Baan R, Grosse Y, Straif K, et al. A review of human carcinogens—part F: chemical agents and related occupations. Lancet Oncol 2009; 10: 1143–4.
- 25Müller AMS, Ihorst G, Mertelsmann R, et al. Epidemiology of non-Hodgkin's lymphoma (NHL): trends, geographic distribution, and etiology. Ann Hematol 2005; 84: 1–12.
Citing Literature
